Mitochondrial abnormalities: A primary basis for oxidative damage in Alzheimer's disease

Drug Development Research

Volumn 46, Issue 1, 1999, Pages 26-33

  Smith, Mark A ^a   Hirai, Keisuke ^a   Nunomura, Akihiko ^a,b   Perry, George ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

Author keywords

Alzheimer's disease; Mitochondrial abnormalities; Oxidative damage

Indexed keywords

ALPHA TOCOPHEROL; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; DAPSONE; ESTROGEN; GINKGO BILOBA EXTRACT; LEVACECARNINE; METAL; MITOCHONDRIAL DNA; NONSTEROID ANTIINFLAMMATORY AGENT; PRESENILIN 1; PRESENILIN 2; REACTIVE OXYGEN METABOLITE; SELEGILINE; TENILSETAM;

AGING; ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BIOACCUMULATION; GENETIC ASSOCIATION; HUMAN; MITOCHONDRION; NEUROPATHOLOGY; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION;

EID: 0032929932     PISSN: 02724391     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2299(199901)46:1<26::AID-DDR5>3.0.CO;2-8     Document Type: Article

References (126)

1. Alonso AC, Zaidi T, Grundke-Iqbal I, Iqbal K. 1994. Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer's disease. Proc Natl Acad Sci USA 91:5562-5566.
2. Alonso AC, Grundke-Iqbal I, Iqbal K. 1996. Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med 2:783-787.
3. Baynes JW. 1991. Role of oxidative stress in development of complications in diabetes. Diabetes 40:405-412.
4. Behl C, Davis J, Cole GM, Schubert D. 1992. Vitamin E protects nerve cells from amyloid-β protein toxicity. Biochem Biophys Res Commun 186:944-950.
5. Behl C, Davis JB, Lesley R, Schubert D. 1994. Hydrogen peroxide mediates amyloid-β protein toxieity. Cell 77:817-827.
6. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F. 1997. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
7. Berlin V, Haseltine WA. 1981. Reduction of adriamycin to a semi-quinone-free radical by NADPH cytochrome P-450 reductase produces DNA cleavage in a reaction mediated by molecular oxygen. J Biol Chem 256:4747-4756.
8. Blass JP, Baker AC, Ko L, Black RS. 1990. Induction of Alzheimer antigens by an uncoupler of oxidative phosphorylation. Arch Neurol 47:864-869.
9. Breitner JCS, Gau BA, Welsh KA, Plassman BL, McDonald WM, Helms MJ, Anthony J. 1994. Inverse association of anti-inflammatory treatments and Alzheimer's disease: initial results of a co-twin control study. Neurology 44:227-232.
10. Butterfield DA, Hensley K, Harris M, Mattson M, Carney J. 1994. β-amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease. Biochem Biophys Res Commun 200:710-715.
11. Carette B, Poulain P, Delacourte A. 1993. Electrophysiological effects of 25-35 amyloid-β-protein on guinea-pig lateral septal neurons. Neurosci Lett 151:111-114.
12. Colaco CA, Ledesma MD, Harrington CR, Avila J. 1996. The role of the Maillard reaction in other pathologies: Alzheimer's disease. Nephrol Dial Transplant 11(Suppl 5):7-12.
13. Colton CA, Gilbert DL. 1987. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 223:284-288.
14. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA. 1993. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
15. Corral-Debrinski M, Horton T, Lott MT, Shoffner JM, McKee AC, Beal MF, Graham BH, Wallace DC. 1994. Marked changes in mitochondrial DNA deletion levels in Alzheimer brains. Genomics 23:471-476.
16. Cotman CW, Su JH. 1996. Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol 6:493-506.
17. Cras P, Kawai M, Siedlak S, Mulvihill P, Gambetti P, Lowery D, Gonzalez-DeWhitt P, Greenberg B, Perry G. 1990. Neuronal and microglial involvement in β-amyloid protein deposition in Alzheimer's disease. Am J Pathol 137:241-246.
18. Davis RE, Miller S, Herrnstadt C, Ghosh SS, Fahy E, Shinobu LA, Galasko D, Thal LJ, Beal MF, Howell N, Parker WD Jr. 1997. Mutations in mitochondrial cytochrome c oxidase genes segregate with late-onset Alzheimer disease. Proc Natl Acad Sci USA94:4526-4531.
19. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD. 1996. Scavenger receptor-mediated adhesion of microglia to β-amyloid fibrils. Nature 382:716-719.
20. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyer B, Soriano F, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J. 1995. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527.
21. Gardner AM, Johnson GL. 1996. Fibroblast growth factor-2 suppression of tumor necrosis factor alpha-mediated apoptosis requires Ras and the activation of mitogen-activated protein kinase. J Biol Chem 271:14560-14566.
22. Goedert M, Sisodia SS, Price DL. 1991. Neurofibrillary tangles and beta-amyloid deposits in Alzheimer's disease. Curr Opin Neurobiol 1:441-447.
23. Good PF, Perl DP Bierer LM, Schmeidler J. 1992. Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study. Ann Neurol 31:286-292.
24. Good PF, Werner P Hsu A, Olanow CW, Perl DP 1996. Evidence of neuronal oxidative damage in Alzheimer's disease. Am J Pathol 149:21-28,
25. Goodman Y, Steiner MR, Steiner SM, Mattson MR 1994. Nordi-hydroguaiaretic acid protects hippocampal neurons against amyloid beta-peptide toxicity, and attenuates free radical and calcium accumulation. Brain Res 654:171-176.
26. Greenberg SG, Davies P Schein JD, Binder LI. 1992. Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 267:564-569.
27. Gustke N, Steiner B, Mandelkow EM, Biernat J, Meyer HE, Goedert M, Mandelkow E. 1992. The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. FEBS Lett 307:199-205.
28. 2. role in cell survival following oxidant injury. J Biol Chem 271:4138-4142.
29. Hamburger SA, McCay PB. 1990. Spin trapping of ibuprofen radicals: evidence that ibuprofen is a hydroxyl radical scavenger. Free Radic Res Commun 9:337-342.
30. Harman D. 1956. Ageing: a theory based on free radical and radiation chemistry. J Gerontol 11:298-300.
31. Harris ME, Carney JM, Cole PS, Hensley K, Howard BJ, Martin L, Bummer P, Wang Y, Pedigo NWJ, Butterfield DA. 1995. β-amyloid peptide-derived, oxygen-dependent free radicals inhibit glutamate uptake in cultured astrocytes: implications for Alzheimer's disease. Neuroreport 6:1875-1879.
32. Henderson VW. 1997. The epidemiology of estrogen replacement therapy and Alzheimer's disease. Neurology 48(Suppl 7):S27-S35.
33. Hensley K, Carney JM, Mattson MP, Aksenova M, Harris M, Wu JF, Floyd RA, Butterfield DA. 1994. A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc Natl Acad Sci USA 91:3270-3274.
34. Hirai K, Smith MA, Wade R, Perry G. 1998a. Vulnerable neurons in Alzheimer disease accumulate mitochondrial DNA with the common 5kb deletion. J Neuropathol Exp Neurol 57:511.
35. Hirai K, Smith MA, Wade R, Perry C. 1998b. Neuronal RNA oxidation and mitochondrial proliferation denote profound metabolic abnormalities in Alzheimer disease. Neurobiol Aging 19 (Suppl 45):54-55.
36. Hirano M, Shtilbans A, Mayeux R, Davidson MM, DiMauro S, Knowles JA, Schon EA. 1997. Apparent mtDNA heteroplasmy in Alzheimer's disease patients and in normals due to PCR amplification of nucleus-embedded mtDNA pseudogenes. Proc Natl Acad Sci USA 94:14894-14899.
37. Hsiao K, Chapman P Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G. 1996. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
38. Hutchin TP, Heath PR, Pearson RC, Sinclair AJ. 1997. Mitochondrial DNA mutations in Alzheimer's disease. Biochem Biophys Res Commun 241:221-225.
39. Hyman BT, Elvhage TE, Reiter J. 1994. Extracellular signal regulated kinases: localization of protein and mRNA in the human hippocampal formation in Alzheimer's disease. Am J Pathol 144:565-572.
40. Igawa K, Maruyama R, Katayama I, Nishioka K. 1997. Anti-oxidative therapy with oral dapsone improved HCV antibody positive annular elastolytic giant cell granuloma. J Dermatol 24:328-331.
41. Iqbal K, Zaidi T, Bancher C, Grundke-Iqbal I. 1994. Alzheimer paired helical filaments: restoration of the biological activity by dephosphorylation. FEBS Lett 349:104-108.
42. Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT. 1997a. APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CAl. J Neuropathol Exp Neurol 56:965-973.
43. Irizarry MC, Soriano F, McNamara M, Page KJ, Schenk D, Games D, Hyman BT. 1997b. Aβ deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J Neurosci 17:7053-7059.
44. Iversen LL, Mortishire-Smith RJ, Pollack SJ, Shearman MS. 1995. The toxicity in vitro of β-amyloid protein. Biochem J 331:1-16.
45. Jones LH, Abdalla DS, Freitas JC. 1995. Effects of indole-3-acetic acid on croton oil- and arachidonic acid-induced mouse ear edema. Inflamm Res 44:372-375.
46. Kanowski S, Herrmann WM, Stephan K, Wierich W, Horr R. 1996. Proof of efficacy of the Ginkgo biloba special extract EGb 761 in outpatients suffering from mild to moderate primary degenerative dementia of the Alzheimer type or multi-infarct dementia. Pharmacopsychiatry 29:47-56.
47. Katzman R. 1986. Alzheimer's disease. N Engl J Med 314:964-973.
48. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A, Bacal C, Lingle DD, Metter E. 1997. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. Neurology 48:1517-1521.
49. Koh JY, Yang LL, Cotman CW. 1990. β-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res 533:315-320.
50. Ledesma MD, Correas I, Avila J, Diaz-Nido J. 1992. Implication of brain cdc2 and MAP2 kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Lett 308:218-224.
51. Ledesma MD, Bonay P, Colaco C, Avila J. 1994. Analysis of microtubule-associated protein tau glycation in paired helical filaments. J Biol Chem 269:21614-21619.
52. 25-35 peptide-mediated neurotoxicity in rat hippocampal cultures. J Neurosci Res 39:494-505.
53. Mattson MR Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE. 1992. β-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
54. McGeer PL, Rogers J. 1992. Anti-inflammatory agents as a therapeutic approach to Alzheimer's disease. Neurology 42:447-449.
55. McLachlan DR, Kruck TR Lukiw WJ, Krishnan SS. 1991. Would decreased aluminum ingestion reduce the incidence of Alzheimer's disease? Can Med Assoc 145:793-804.
56. McShea A, Harris PLR, Webster KR, Wahl A, Smith MA. 1997. Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am J Pathol 150:1933-1939.
57. McShea A, Wahl AF, Smith MA. 1999. Re-entry into the cell cycle: a mechanism for neurodegeneration in Alzheimer disease. Med Hypotheses, in press.
58. Miyata M, Smith JD. 1996. Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and β-amyloid peptides. Nat Genet 14:55-61.
59. Montine TJ, Amarnath V, Martin ME, Strittmatter WJ, Graham DG. 1996a. E-4-hydroxy-2-nonenal is cytotoxic and cross-links cytoskeletal proteins in P19 neuroglial cultures. Am J Pathol 148:89-93.
60. Montine TJ, Huang DY, Valentine WM, Amarnath V, Saunders A, Weisgraber KH, Graham DG, Strittmatter WJ. 1996b. Crosslinking of apolipoprotein E by products of lipid peroxidation. J Neuropathol Exp Neurol 55:202-210.
61. Münch G, Taneli Y, Schraven E, Schindler U, Schinzel R, Palm D, Riederer P. 1994. The cognition-enhancing drag tenilsetam is an inhibitor of protein crosslinking by advanced glycosylation. J Neural Trans-Parkinsons Dis Dem Sect 8:193-208.
62. Münch G, Mayer S, Michaelis J, Hipkiss AR, Riederer P, Muller R, Neumann A, Schinzel R, Cunningham AM. 1997. Influence of advanced glycation end-products and AGE-inhibitors on nucleation-dependent polymerization of beta-amyloid peptide. Biochim Biophys Acta 1360:17-29.
63. Neuzil J, Witting PK, Stocker R. 1997. Alpha-tocopheryl hydro-quinone is an efficient multifunctional inhibitor of radical-initiated oxidation of low density lipoprotein lipids. Proc Natl Acad Sci USA 94:7885-7890.
64. Oteiza PI. 1994. A mechanism for the stimulatory effect of aluminum on iron-induced lipid peroxidation. Arch Biochem Biophys 308:374-379.
65. Papasozomenos SC. 1997. The heat shock-induced hyperphosphorylation of tau is estrogen-independent and prevented by androgens: implications for Alzheimer disease. Proc Natl Acad Sci USA 94:6612-6617.
66. Pappolla MA, Omar RA, Kim KS, Robakis NK. 1992. Immunohistochemical evidence of oxidative stress in Alzheimer's disease. Am J Pathol 140:621-628.
67. Pappolla M, Chyan Y-J, Omar RA, Hsiao K, Perry G, Smith MA, Bozner P. 1998. Evidence of oxidative stress and in vivo neurotoxicity of β-amyloid in a transgenic mouse model of Alzheimer's disease: a chronic oxidative paradigm for testing antioxidant therapies in vivo. Am J Pathol 152:871-877.
68. Parker WD Jr, Filley CM, Parks JK. 1990. Cytochrome oxidative deficiency in Alzheimer's disease. Neurology 40:1302-1303.
69. Perry G, Kawai M, Tabaton M, Onorato M, Mulvihill P, Richey P, Morandi A, Connolly JA, Gambetti P. 1991. Neuropil threads of Alzheimer's disease show a marked alteration of the normal cytoskeleton. J Neurosci 11:1748-1755.
70. Pope WB, Lambert MP, Leypold B, Seupaul R, Sletten L, Krafft G, Klein WL. 1994. Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY5Y Exp Neurol 126:185-194.
71. Praprotnik D, Smith MA, Richey PL, Vinters HV, Perry G. 1996a. Plasma membrane fragility in dystrophic neuntes in senile plaques of Alzheimer's disease: an index of oxidative stress. Acta Neuropathol 91:1-5.
72. Praprotnik D, Smith MA, Richey PL, Vinters HV, Perry G. 1996b. Filament heterogeneity within the dystrophic neuntes of senile plaques suggests blockage of fest axonal transport in Alzheimer's disease. Acta Neuropathol 91:226-235.
73. Prehn JH, Bindokas VP, Jordan J, Galindo MF, Ghadge GD, Roos RP, Boise LH, Thompson CB, Krajewski S, Reed JC, Miller RJ. 1996. Protective effect of transforming growth factor-β1 on β-amyloid neurotoxicity in rat hippocampal neurons. Mol Pharmacol 49:319-328.
74. Premkumar DRD, Smith MA, Richey PL, Petersen RB, Castellani R, Kutty RK, Wiggert B, Perry G, Kalaria RN. 1995. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J Neurochem 65:1399-1402.
75. Preuss U, Doting F, Illenberger S, Mandelkow EM. 1995. Cell cycle-dependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol Biol Cell 6:1397-1410.
76. Rich JB, Rasmusson DX, Folstein MF, Carson KA, Kawas C, Brandt J. 1995. Nonsteroidal anti-inflammatory drugs in Alzheimer's disease. Neurology 45:51-55.
77. Ripple MO, Henry WF, Rago RP, Wilding G. 1997. Prooxidant-antioxidant shift induced by androgen treatment of human prostate carcinoma cells. J Natl Cancer Inst 89:40-48.
78. Rogers J, Kirby LC, Hempelman SR, Berry DL, McGeer PL, Kaszniak AW, Zalinski J, Cofield M, Mansukhani L, Willson P, Kogan F. 1993. Clinical trial of indomethacin in Alzheimer's disease. Neurology 43:1609-1611.
79. Rong Y, Geng Z, Lau BH. 1996. Ginkgo biloba attenuates oxidative stress in macrophages and endothelial cells. Free Radic Biol Med 20:121-127.
80. Roses AD. 1995. On the metabolism of apolipoprotein E and the Alzheimer diseases. Exp Neurol 132:149-156.
81. Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury E Growdon J, Cotman CW, Pfeiffer E, Schneider LS, Thal LJ. 1997. A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N Engl J Med 336:1216-1222.
82. Sayre LM, Zelasko DA, Harris PLR, Perry G, Salomon RG, Smith MA. 1997a, 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68:2092-2097.
83. Sayre LM, Zagorski MG, Surewicz WK, Krafft GA, Perry G. 1997b. Mechanisms of neurotoxicity associated with amyloid β deposition and the role of free radicals in the pathogenesis of Alzheimer's disease: a critical appraisal. Chem Res Toxicol 10:518-526.
84. Schinetti ML, Rossini D, Greco R, Bertelli A. 1987. Protective action of acetylcarnitine on NADPH-induced lipid peroxidation of cardiac microsomes. Drugs Exp Clin Res 13:509-515.
85. Schipper HM, Cisse S, Stopa EG. 1995. Expression of heme oxygenase-1 in the senescent and Alzhemer-diseased brain. Ann Neurol 37:758-768.
86. Schreck R, Rieber P, Baeuerle PA. 1991. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J 10:2247-2258.
87. Selkoe DJ. 1997. Alzheimer's disease: genotypes, phenotypes, and treatments. Science 275:630-631.
88. Selkoe DJ, Ihara Y, Salazar FJ. 1982. Alzheimer's disease: insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea. Science 215:1243-1245.
89. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K, Tsuda T, Mar L, Foncin J-F, Bruni AC, Montesi MP, Sorbi S, Rainero I, Pinessi L, Polinsky RJ, Wasco W, Da Silva HAR, Haines JL, Pericak-Vance MA, Tanzi RE, Roses AD, Fraser PE, Rommens JM, St. George-Hyslop PH. 1995. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375:754-760.
90. Sheu KF, Kim YT, Blass JP, Weksler ME. 1985. An immunochemical study of the pyruvate dehydrogenase deficit in Alzheimer's disease brain. Ann Neurol 17:444-449.
91. Shoda H, Miyata S, Liu BF, Yamada H, Ohara T, Suzuki K, Oimomi M, Kasuga M. 1997. Inhibitory effects of tenilsetam on the Maillard reaction. Endocrinology 138:1886-1892.
92. Sims NR, Finegan JM, Blass JP, Bowen DM, Neary D. 1987. Mitochondrial function in brain tissue in primary degenerative dementia. Brain Res 436:30-38.
93. Skolnick AA. 1997. Old Chinese herbal medicine used for fever yields possible new Alzheimer disease therapy. J Am Med Assoc 277:776.
94. Smalheiser NR, Swanson DR. 1996. Indomethacin and Alzheimer's disease. Neurology 46:583.
95. Smith MA. 1998. Alzheimer disease. In: Bradley JY, Harris RA, editors. International Review of Neurobiology. San Diego: Academic Press. p 1-54.
96. Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, Marksberry WR. 1991. Excess brain protein oxidative and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci USA 88:10540-10543.
97. Smith MA, Taneda S, Richey PL, Miyata S, Van S-D, Stern D, Sayre LM, Monnier VM, Perry G. 1994a. Advanced Maillard reaction products are associated with Alzheimer disease pathology. Proc Natl Acad Sci USA 91:5710-5714.
98. Smith MA, Kutty RK, Richey PL, Yan S-D, Stern D, Chader GJ, Wiggert B, Petersen RB, Perry G. 1994b. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am J Pathol 145:42-47.
99. Smith MA, Sayre LM, Monnier VM, Perry G. 1995a. Radical AGEing in Alzheimer's disease. Trends Neurosci 18:172-176.
100. Smith MA, Rudnicka-Nawrot M, Richey PL, Praprotnik D, Mulvihill P, Miller CA, Sayre LM, Perry G. 1995b. Carbonyl-related post-translational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease. J Neurochem 64:2660-2666.
101. Smith MA, Sayre LM, Vitek MP, Monnier VM, Perry G. 1995c. Early AGEing and Alzheimer's. Nature 374:316.
102. Smith MA, Perry G, Richey PL, Sayre LM, Anderson VE, Beal MF, Kowall N. 1996a. Oxidative damage in Alzheimer's. Nature 382:120-121.
103. Smith MA, Siedlak SL, Richey PL, Nagaraj RH, Elhammer A, Perry G. 1996b. Quantitative solubilization and analysis of insoluble paired helical filaments from Alzheimer disease. Brain Res 717:99-108.
104. Smith MA, Harris PLR, Sayre LM, Beckman JS, Perry G. 1997a. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17:2653-2657.
105. Smith MA, Harris PLR, Sayre LM, Perry G. 1997b. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci USA 94:9866-9868.
106. Smith MA, Vašák M, Knipp M, Castellani RJ, Perry G. 1998a. Dimethylargininase, a nitric oxide regulatory protein, in Alzheimer disease. Free Radic Biol Med 25:898-902.
107. Smith MA, Hirai K, Hsiao K, Pappolla MA, Harris PLR, Siedlak SL, Tabaton M, Perry G. 1998b. Amyloid-β deposition in Alzheimer transgenic mice initiates oxidative stress. J Neurochem 70:2212-2215.
108. Sorbi S, Bird ED, Blass JP. 1983. Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain. Ann Neurol 13:72-78.
109. Stewart WF, Kawas C, Corrada M, Metter EJ. 1997. Risk of Alzheimer's disease and duration of NSAID use. Neurology 48:626-631.
110. Stoll S, Scheuer K, Pohl O, Muller WE. 1996. Ginkgo biloba extract (EGb 761) independently improves changes in passive avoidance learning and brain membrane fluidity in the aging mouse. Pharmacopsychiatry 29:144-149.
111. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, Roses AD. 1993. Binding of human apolipoprotein E to synthetic amyloid β peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:8098-8102.
112. Su JH, Anderson AJ, Cummings BJ, Cotman CW. 1994. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5:2529-2533.
113. Thal LJ, Carta A, Clarke WR, Ferris SH, Friedland RP, Petersen RC, Pettegrew JW, Pfeiffer E, Raskind MA, Sano M, Tuszynski MH, Woolson RF. 1996. A 1-year multicenter placebo-controlled study of acetyl-L-carnitine in patients with Alzheimer s disease. Neurology 47:705-711.
114. Trojanowski JQ, Schmidt ML, Shin R-W, Bramblett GT, Goedert M, Lee VM-Y. 1993a. PHF-τ (A68): from pathological marker to potential mediator of neuronal dysfunction and degeneration in Alzheimer's disease. Clin Neurosci 1:184-191.
115. Trojanowski JQ, Mawal-Dewan M, Schmidt ML, Martin J, Lee VM. 1993b. Localization of the mitogen activated protein kinase ERK2 in Alzheimer's disease neurofibrillary tangles and senile plaque neurites. Brain Res 618:333-337.
116. Vane JR, Botting RM. 1997. Mechanism of action of aspirin-like drugs. Semin Arthritis Rheum 26(6 Suppl 1):2-10.
117. Vincent I, Rosado M, Davies P. 1996. Mitotic mechanisms in Alzheimer's disease? J Cell Biol 132:413-425.
118. Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, Manogue K, Cerami A. 1994. Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc Natl Acad Sci USA 91:4766-4770.
119. Wallace DC, Stugard C, Murdock D, Schurr T, Brown MD. 1997. Ancient mtDNA sequences in the human nuclear genome: a potential source of errors in identifying pathogenic mutations. Proc Natl Acad Sci USA 94:14900-14905.
120. Wolozin B, Iwasaki K, Vito P, Ganjei JK, Lacana E, Sunderland T, Zhao B, Kusiak JW, Wasco W, D'Adamio L. 1996. Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation. Science 274:1710-1713.
121. Wu RM, Murphy DL, Chiueh CC. 1996. Suppression of hydroxyl radical formation and protection of nigral neurons by 1-deprenyl (selegiline). Ann NY Acad Sci 786:379-390.
122. Yan S-D, Chen X, Schmidt A-M, Brett J, Godman G, Zou Y-S, Scott CW, Caputo C, Frappier T, Smith MA, Perry G, Yen S-H, Stern D. 1994. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc Natl Acad Sci USA 91:7787-7791.
123. Yan SD, Yan SF Chen X, Fu J, Chen M, Kuppusamy P, Smith MA, Perry G, Godman GC, Nawroth P Zweier JL, Stern D. 1995. Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid β-peptide. Nat Med 1:693-699.
124. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P Stern D, Schmidt AM. 1996. RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
125. Yankner BA, Duffy LK, Kirschner DA. 1990. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250:279-282.
126. 2 generation. J Neurochem 67:1595-1606.